A secreted Botrytis cinerea stage-specific effector promotes virulence by targeting the plant ROS-generating machinery

Abstract

Necrotrophic plant pathogens are assumed to exploit the plant hypersensitive response (HR), but the molecular mechanism underlying this exploitation remains largely unclear. Here, we report the discovery and characterization of BcCELP1, an early infection-specific, cell death-inducing effector required for plant colonization by the phytopathogenic fungus Botrytis cinerea. We demonstrate that BcCELP1 is necessary during the initial stage of plant colonization, and that it interacts with the host scaffold protein NbRACK1, promoting NbRACK1’s interaction with the reduced nicotinamide adenine dinucleotide phosphate oxidase NbRBOHB, and thereby contributing to excessive ROS production. We further show that BcCELP1 is produced and specifically leveraged during plant invasion to facilitate the formation of necrotic tissue patches, which serve as foci for subsequent fungal spread. Misregulation of bccelp1 disrupts pathogen development, resulting in reduced disease symptoms. Collectively, these findings reveal an unsuspected sophisticated strategy employed by a necrotrophic pathogen, whereby a fungal effector activates the host ROS-generating machinery in a stage-specific manner to promote effective invasion.